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SOME ASPECTS of NUCLEIC ACID Ia2>TD PROTEIN SYNTHESIS IN

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SOME ASPECTS of NUCLEIC ACID Ia2>TD PROTEIN SYNTHESIS IN SOME ASPECTS OF NUCLEIC ACID iA2>TD PROTEIN SYNTHESIS IN CELL NUCLEI DISSERTATION Presented in Partial Fulfillment of the Requirements for -trhe Degree Doctor of philosophy in the Graduate School of The Ohio State University By TEiEODORE RONALD BREITMAN, B. S., M. S. ****** The Ohio State University 1958 Approved by dviser Department of Agricultural Biochemistry Ack no w 1 e dgme n t s The author wishes to express his appreciation to Dr. George C. Webster for his counsel and guidance throughout the course of this investigation. A special note of thanks goes to Dr. Ruth G. Kleinfeld for her collaboration in the thioacetamide experiments. iii Table of Contents Page Introduction ......................................... 1 Studies on Nuclear Metabolism in vivo ...... 1 a. Ribonucleic Acid............... ....... 1 b. Deoxyribonucleic Acid............... 4 c. Protein...... 6 Studies on Nuclear Metabolism in vitro. a. Ribonucleic Acid..... eoaaaoaoooaoa* b. Deoxyribonucleic Acid.................. 13 c. Protein.......... 15 Aims of this Investigation...................... 21 E xp e r 1 me ntalo..ooo.....................««.««.«..«.oo«23 Methods.................... 23 Results ............... 25 Effects of Monovalent Cations........ 25 Time Course of B 3* Incorporation into RNA. ...................... 31 Inhibitor Studies......... 31 The Effect of Thioacetamj.de on Nuclear RNA Metabolism in vivo......... 41 Effect of Thioacetamide on Isolated Thymus Nuclei....... 46 Discussion..eo.o..o.oo«.....o.ooo.ooo........ ........ 48 Summary.................«o.. o..oo.o q . o »o.o.oooo. o.... oO Bibliography...............ooo....oooo.o.oo.ooo.oo.ooo2 A.U tOb lO gr aphy oo«o«ooo....ooooo>oe.«*.oo.oo.o.ooooo»...35 iv List of Tables P age Table 1. Incorporation of the Carbon or Phosphorus of Various Labeled Compounds into Nuclear RN'A, DiSfA, or Protein......... 25 Table 2. Effect of Replacement of Sodium by Potassium Ions on the Incorporation of Various Precursors into Nuclear RNA, DNA, and Protein................ 27 Table 3. Effect of Partial Replacement of Sodium Ions by Various Monovalent Cations on Glycine Carbon Incorporation into RMA, DNA, and Protein.................... 30 V List of Figures Page Figure 1. Inhibition of the incorporation of glycine carbon into nuclear Rl\iA, DNA., and protein by progressive replacement of sodium by potassium ions........... 29 Figure 2. Time course of P incorporation into the iltJA of isolated thymus nuclei..... 32 1 A Figure 3. Effect of chloramphenicol on alanine-C incorporation into protein and ortho- phosphate-p32incorporation into RNA and DMA. ................................................................................... 34 Figure 4. Effect of purine and S-mereaptopurine on the incorporation of glycine carbon into nuclear RMA, DMA, and protein............ 33 Figure 5. Effect of amino acid analogs on the incorporation of glycine carbon into nuclear RIIA, DLSFA, and protein......» ...... 37 Figure 5. Effects of ribonuclease and deoxyribo­ nuclease on the incorporation of glycine carbon into nuclear RjtfA* DMA, and protein. „.............. ................ Figure 7., Effects of varying concentrations of RiSl'Aase on the incorporation of glycine carbon into nuclear RNA and protein.... 40 Figure S. Specific activitv/DNA/RNA-tiiae curves for nuclear RNA. ....... ........... 42 Figure 9. Specific activity/DNA/RNA-time curves for nuclear RNA. .............,, 44 Figure 10. Effect of TA on the DNA/RNA ratios...... 45 • i 4 Figure 11. Effect of TA on alanine-CJ" incorporation into the protein of isolated thymus nuclei......... ........................... 47 1 Introduction The cell nucleus, because of its active role in cellu­ lar division and its presence in most animal and plant cells, has been actively studied by the cytologist for some time. The biochemist's interest in events taking place in the nucleus was seriously hampered by the lack of techniques for both isolating and analyzing the nucleus for its constituents. The advent of methods for breaking up tissue and isolating cellular components has made possible, as with other cellular entities, the more intimate mode of investigation that we are familiar with today. It would be redundant to review here the vast number of papers dealing with the biochemistry of the nucleus. Many excellent reviews are available which treat the vari­ ous areas of this growing field (1-7). It would, however, be within the scope of this introduction to review briefly those aspects of nuclear metabolism which bear closely to the contents of this dissertation. Studies on Nuclear Metabolism in vivo a. Ribonucleic Acid (RNA) With the availability of isotopes, it became possible to study intermediary metabolism at a level of sensitivity never before thought possible. Such studies using a vari­ ety of isotopically labeled precursors (e.g., phosphate la- 32 14 beled P , C -formate and a diversity of amino acids, pu­ rines, pyrimidines, nucleotides, and nucleosides labeled 35 15 with radiocarbon, tritium, S , and/or N ) have made it clear that the RNA of the nucleus has a marked metabolic 32 activity. In 1948 Marshak (8), using P and Bergstrand 15 et al. (9), using glycine-N , reported that more of these isotopes were incorporated into the nuclear RNA than was taken up by the cytoplasmic RNA, an observation which has since been confirmed in many other laboratories using a variety of isotopes and materials (10-19). Such evidence led several workers to propose that the nuclear RNA is the precursor of cytoplasmic RNA (10,20). on the other hand, it has been proposed by Barnura et al. (12,13) that the nucleus and cytoplasm synthesize RNA independently, the nuclear rate being higher. Another objection to the pro­ posed precursor role of nuclear RNA is based on the ob­ served differences in the nucleotide composition of nuclear RNA and cytoplasmic RNA when compared in bulk (21-23) . This would appear to obviate the possibility that nuclear RNA could simply diffuse into the cytoplasm. More recently, it has been reported that a nuclear RNA fraction, soluble in neutral phosphate buffer, has the same nucleotide compo­ sition and electrophoretic mobility as that of cytoplasmic 32 RNA and incorporates p into its mixed nucleotides at a substantially greater rate than does the corresponding cytoplasmic RNA (24,25). However, these results are not entirely in accord with an earlier paper of Logan and Davidson (26) who report differences in composition between the soluble nuclear RNA and the cytoplasmic RNA. Other lines of research have drawn attention to the dependence of cytoplasmic RNA on the activity of the nuc­ leus as shown by comparisons between nucleated and enuc­ leated cells. The researches of Linet and Brachet (27) and of James (28), on Amoeba. agreed in the observation that the RNA level declined in the enucleated portions but tended to be maintained in the nucleated fragments. The results ob­ tained by Goldstein and Plaut (29) clearly demonstrated the transfer of nuclear RNA or its components to the cytoplasm, and gave no indications for the reverse process. Further experiments by Plaut and Rustad (30) indicated that adenine- 14 8-C was incorporated into the RNA of the enucleated por­ tion of Amoeba at a slower rate than into the nucleated portion or into the whole organism. In contrast to these results with Amoeba fragments, which have been interpreted as strongly suggesting a nuclear control on cytoplasmic RNA metabolism, are the results of Brachet and coworkers (31, 32) who have demonstrated in Acetabularia that enucleate fragments can grow, synthesize protein and RNA, and differ­ entiate without a nucleus. These authors have also found that both enucleate and nucleate portions of Acetabularia 14 could incorporate orotic acid-C into their RNA, the nucleated half incorporating 1.4 times as much label as the enucleated half. A more critical experiment on Acetabularia has recently been reported by Stich and Plaut (33). Ribonuclease treated nucleate and enucleate frag­ ments of Acetabularia were investigated for their ability to grow, synthesize protein, and differentiate. It was found that while nucleate portions recovered their capacity in these respects, enucleate fragments did not. The au­ thors have interpreted these results to indicate that some nuclear product was required for recovery and that the product is most probably nuclear RNA. While the results outlined above leave little doubt for the existence of a nuclear mechanism for RNA synthesis, the metabolic role of this constituent in the nucleus and its possible role in other parts of the cell has still to be clearly elucidated. The possibility that RNA or ribo- nucleoprotein plays a role as a mediator of genetic infor­ mation exists (34). Experiments with viruses demonstrate that RNA may in some situations transmit genetic informa­ tion (35,36) . b. Deoxyribonucleic Acid (DNA) It has become a generally accepted observation that DNA is a metabolically stable cellular component, the syn­ thesis of which occurs principally in connection with cel­ lular division. The biochemical researches which have led to this concept were initiated by Hevesy in 1940 (37) and further confirmed and extended in the years immediately following by Brues et al. (38) and Marshak (8) . These in- 32 vestigators showed that the incorporation of P -labeled phosphate into the DNA of various tissues closely paral­ leled the rate of cell division. In resting tissues the 32 rate of P incorporation into DNA-phosphorus is very small 32 but the incorporation
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